diff --git a/.changeset/famous-gorillas-confess.md b/.changeset/famous-gorillas-confess.md
new file mode 100644
index 000000000000..7e12528681a0
--- /dev/null
+++ b/.changeset/famous-gorillas-confess.md
@@ -0,0 +1,5 @@
+---
+'astro': patch
+---
+
+Fixes an issue where `Astro.locals` coming from an adapter weren't available in the `404.astro`, when using the `astro dev` command,
diff --git a/packages/astro/src/vite-plugin-astro-server/route.ts b/packages/astro/src/vite-plugin-astro-server/route.ts
index da4f309dad37..025ba1e75cbe 100644
--- a/packages/astro/src/vite-plugin-astro-server/route.ts
+++ b/packages/astro/src/vite-plugin-astro-server/route.ts
@@ -246,7 +246,7 @@ export async function handleRoute({
 		const fourOhFourRoute = await matchRoute('/404', manifestData, pipeline);
 		if (fourOhFourRoute) {
 			renderContext = await RenderContext.create({
-				locals: {},
+				locals,
 				pipeline,
 				pathname,
 				middleware: isDefaultPrerendered404(fourOhFourRoute.route) ? undefined : middleware,
diff --git a/packages/astro/test/custom-404-locals.test.js b/packages/astro/test/custom-404-locals.test.js
new file mode 100644
index 000000000000..246e9e31e4b0
--- /dev/null
+++ b/packages/astro/test/custom-404-locals.test.js
@@ -0,0 +1,59 @@
+import assert from 'node:assert/strict';
+import { after, before, describe, it } from 'node:test';
+import * as cheerio from 'cheerio';
+import { loadFixture } from './test-utils.js';
+
+describe('Custom 404 locals', () => {
+	let fixture;
+
+	before(async () => {
+		fixture = await loadFixture({
+			root: './fixtures/custom-404-locals/',
+			site: 'http://example.com',
+		});
+	});
+ 
+	describe('dev', () => {
+		let devServer;
+		let $;
+
+		before(async () => {
+			devServer = await fixture.startDevServer();
+		});
+
+		after(async () => {
+			await devServer.stop();
+		});
+
+		it('renders /', async () => {
+			const html = await fixture.fetch('/').then((res) => res.text());
+			$ = cheerio.load(html);
+
+			assert.equal($('h1').text(), 'Home');
+		});
+
+		it('renders 404 for /a', async () => {
+			const res = await fixture.fetch('/a');
+			assert.equal(res.status, 404);
+
+			const html = await res.text();
+			$ = cheerio.load(html);
+
+			assert.equal($('h1').text(), 'Page not found');
+			assert.equal($('p.message').text(), 'This 404 is a dynamic HTML file.');
+			assert.equal($('p.runtime').text(), 'locals');
+		});
+
+		it('renders 404 for /404-return', async () => {
+			const res = await fixture.fetch('/404-return');
+			assert.equal(res.status, 404);
+
+			const html = await res.text();
+			$ = cheerio.load(html);
+
+			assert.equal($('h1').text(), 'Page not found');
+			assert.equal($('p.message').text(), 'This 404 is a dynamic HTML file.');
+			assert.equal($('p.runtime').text(), 'locals');
+		});
+	});
+});
diff --git a/packages/astro/test/fixtures/custom-404-locals/astro.config.mjs b/packages/astro/test/fixtures/custom-404-locals/astro.config.mjs
new file mode 100644
index 000000000000..8e5335b3d5c6
--- /dev/null
+++ b/packages/astro/test/fixtures/custom-404-locals/astro.config.mjs
@@ -0,0 +1,19 @@
+import { defineConfig } from 'astro/config';
+
+// https://astro.build/config
+export default defineConfig({
+	integrations: [{
+		name: 'locals-integration',
+		hooks: {
+			'astro:server:setup': ({ server }) => {
+				server.middlewares.use(async function middleware(req, res, next) {
+						const clientLocalsSymbol = Symbol.for('astro.locals');
+						Reflect.set(req, clientLocalsSymbol, {
+							runtime: 'locals'
+					});
+					next();
+				});
+			},
+		},
+	}]
+});
diff --git a/packages/astro/test/fixtures/custom-404-locals/package.json b/packages/astro/test/fixtures/custom-404-locals/package.json
new file mode 100644
index 000000000000..6fe4651b3a6c
--- /dev/null
+++ b/packages/astro/test/fixtures/custom-404-locals/package.json
@@ -0,0 +1,8 @@
+{
+  "name": "@test/custom-404-locals",
+  "version": "0.0.0",
+  "private": true,
+  "dependencies": {
+    "astro": "workspace:*"
+  }
+}
diff --git a/packages/astro/test/fixtures/custom-404-locals/src/pages/404-return.astro b/packages/astro/test/fixtures/custom-404-locals/src/pages/404-return.astro
new file mode 100644
index 000000000000..85c7644717e6
--- /dev/null
+++ b/packages/astro/test/fixtures/custom-404-locals/src/pages/404-return.astro
@@ -0,0 +1,5 @@
+---
+return new Response(null, { status: 404 });
+---
+
+I should never load
\ No newline at end of file
diff --git a/packages/astro/test/fixtures/custom-404-locals/src/pages/404.astro b/packages/astro/test/fixtures/custom-404-locals/src/pages/404.astro
new file mode 100644
index 000000000000..867ca600c980
--- /dev/null
+++ b/packages/astro/test/fixtures/custom-404-locals/src/pages/404.astro
@@ -0,0 +1,13 @@
+---
+const runtime = Astro.locals.runtime
+---
+<html lang="en">
+<head>
+  <title>Not Found - Custom 404</title>
+</head>
+<body>
+  <h1>Page not found</h1>
+	<p class="message">This 404 is a dynamic HTML file.</p>
+  <p class="runtime">{runtime}</p>
+</body>
+</html>
\ No newline at end of file
diff --git a/packages/astro/test/fixtures/custom-404-locals/src/pages/index.astro b/packages/astro/test/fixtures/custom-404-locals/src/pages/index.astro
new file mode 100644
index 000000000000..cf5ef9b586c6
--- /dev/null
+++ b/packages/astro/test/fixtures/custom-404-locals/src/pages/index.astro
@@ -0,0 +1,11 @@
+---
+---
+
+<html lang="en">
+<head>
+  <title>Custom 404</title>
+</head>
+<body>
+  <h1>Home</h1>
+</body>
+</html>
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index 6279bfc08916..15f9f2303831 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -2888,6 +2888,12 @@ importers:
         specifier: workspace:*
         version: link:../../..
 
+  packages/astro/test/fixtures/custom-404-locals:
+    dependencies:
+      astro:
+        specifier: workspace:*
+        version: link:../../..
+
   packages/astro/test/fixtures/custom-404-loop-case-1:
     dependencies:
       astro: